© 2015 American Society of Plant Biologists
JASMONATES
© 2015 American Society of Plant Biologists
Plants are surrounded by many
enemies with a common goal...
Photo by Gilbert Ahlstrand courtesy USDA, Photo by Eric Erbe, digital colorization by Christopher Pooley, http://www.inra.fr/meloidogyne_incognita, D'Arcy, C. J. , D.
M. Eastburn, and G. L. Schumann. 2001. Illustrated Glossary of Plant Pathology. The Plant Health Instructor
Insects
Fungi
Bacteria
Oomycetes
Nematodes
... to “eat” them!
© 2015 American Society of Plant Biologists
Pathogens and pests cause
significant crop losses
Images courtesy Clemson University - USDA Cooperative Extension Slide Series, Bugwood.org;
Charles Averre, North Carolina State University, Bugwood.org
Jasmonates and salicylates
are hormones that participate
in plant defense responses
Most plants are
resistant to most pests,
but a few organisms
cause tremendous
damage. 25% or more of
potential harvests can be lost
to insects and disease!
European corn borer
Ostrinia nubilalis
in its host Zea mays
Phytophthora capsici on
cucumber (Cucumis sativus)
© 2015 American Society of Plant Biologists
Microorganisms are
(hemi)biotrophic or necrotrophic
Cell death
accompanies or
precedes
colonization by
necrotrophs
Biotrophs or hemibiotrophs
can live within their host
tissue without causing
(immediate) death
Toxin Pseudomonas
syringae in
intracellular space
Bestwick, C.S., Brown, I.R., Bennett, M., and Mansfield, J.W. (1997). Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells
to Pseudomonas syringae pv phaseolicola. Plant Cell 9: 209-221.
© 2015 American Society of Plant Biologists
Insects eat leaves, flowers, seeds
and roots and spread diseases
Boll weevil (Anthonomus grandis
grandis) on cotton (Gossypium hirsutum)
Leaf beetle (Phratora laticollis) on
European aspen (Populus tremula)
Image credits: Petr Kapitola, State Phytosanitary Administration, Bugwood.org ; Alton N. Sparks, Jr., University of Georgia, Bugwood.org
© 2015 American Society of Plant Biologists
Jasmonates participate in plant
defenses to insects and necrotrophs
Jasmonates Salicylates
Transcriptional
responses
To a first
approximation, insects
and necrotrophs trigger
jasmonate production,
and biotrophs trigger
salicylate production
© 2015 American Society of Plant Biologists
Jasmonates also contribute to
developmental and growth controls
Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E., and Howe, G.A. (2004). The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed
maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143; Reprinted by permission from Macmillan Publishers Ltd. Thines, B., Katsir, L., Melotto, M., Niu, Y.,
Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665.
JA also controls: cell cycle, root
extension, leaf senescence,
stomata closure, and mutualistic
interactions....
Trichome formation Seed development Flower development
© 2015 American Society of Plant Biologists
Lecture outline
• Jasmonate biochemistry
• Jasmonate signaling: • COI1- JAZ coreceptor
• JAZ repressors
• Transcriptional responses
• Jasmonates in whole-plant processes: • Responses to insects
• Responses to pathogens and other microorganisms
• Cross-talk in defense signaling
• Jasmonates in development and other functions
© 2015 American Society of Plant Biologists
Jasmonates – synthesis, conjugation,
transport and degradation
Demole, E. Lederer, E., and Mercier, D. (1962) Isolement et détermination de la structure du jasmonate de méthyle, constituant odorant charactéristique de l’èssence de
jasmin. Helv. Chim. Acta 45: 675 -685.
Like other esters, methyl jasmonate smells good – it is the dominant scent
from jasmine flowers
“Jasmonate de méthyle”
O
CH2COOCH3
Methyl jasmonate was purified from Jasminum grandiflorium in 1962
© 2015 American Society of Plant Biologists
Jasmonates include jasmonic acid
(JA) and derivatives
JA-Ile
OH
(3R,7S)-jasmonic acid
a.k.a.
(+)-7-iso-jasmonic acid
Jasmonic acid
(JA) JA-Isoleucine
(JA-Ile)
OCH3
Methyl jasmonate
(MeJA)
Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W., Luo, H., Nan, F., Wang, Z., and Xie, D. (2009). The Arabidopsis CORONATINE
INSENSITIVE1 protein Is a jasmonate receptor. Plant Cell 21: 2220-2236.
© 2015 American Society of Plant Biologists
Jasmonates are produced preventively in
flowers and induced as a defense response
in other tissues
Gundlach, H., Müller, M.J., Kutchan, T.M., and Zenk, M.H. (1992). Jasmonic acid is a signal transducer in elicitor-induced plant cell cultures. Proc. Natl. Acad. Sci. 89: 2389-2393. (Photo from Wikipedia)
Wounding, pathogens or herbivores (or
molecules derived from them) trigger very
rapid accumulation of jasmonates
JA
MeJA
Untreated control
Induction of
jasmonate production
in cell suspension
culture (Rauvolfia
canescens, a
medicinal plant) by
adding yeast cell wall
elicitor
Rauvolfia canescens
© 2015 American Society of Plant Biologists
JA accumulates in a circadian
pattern in phase with herbivory
Resistance to herbivory decreases when
Arabidopsis cycles out-of-phase to the insects
Reprinted from Goodspeed, D., Chehab, E.W., Min-Venditti, A., Braam, J., Covington, M.F. (2012). Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc. Natl. Acad. Sci. USA 109: 4674-4677.
JA
SA
Herbivory
Hormone accumulation
JA and SA
cycle in
opposite
phasing
© 2015 American Society of Plant Biologists
Jasmonate synthesis occurs in the
plastid, peroxisome and cytosol
LOX
AOS AOC OPDA OPDA OPR3
β-oxidation
JA
MeJA JA-Ile
plastid peroxisome
Lipase
α-linolenic acid (18:3)
(in membrane)
ACX1
cytosol
© 2015 American Society of Plant Biologists
Jasmonate precursors are derived
from membrane lipids
Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. (2001). The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing
the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209.
DAD1, DGL, GLA1
Lipolytic enzymes
are necessary for JA
synthesis and are
under tight regulation
MEMBRANE
Free fatty acid
Lipase Membrane
lipid
Free fatty
acid
α-linolenic acid
© 2015 American Society of Plant Biologists
In Arabidopsis DAD1 and DGL lipases
are expressed in different tissues
Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. (2001). The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen
maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209; Reprinted from Hyun, Y., Choi, S., Hwang, H.-J., Yu, J., Nam, S.-J., Ko, J., Park, J.-Y., Seo, Y.S., Kim, E.Y., Ryu, S.B., Kim, W.T., Lee, Y.-H., Kang,
H., and Lee, I. (2008). Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Developmental Cell 14: 183-192 with permission from Elsevier.
DAD1 is
expressed in
anthers and is
necessary for
male fertility
In Arabidopsis the
DGL lipase is
expressed in rosette
leaves and involved
in wound response
© 2015 American Society of Plant Biologists
Jasmonates are derived from free
fatty acids Linolenic acid has 18 carbons and 3 double bonds
so is called an 18:3 octadecanoid
Another way to draw
linolenic acid
© 2015 American Society of Plant Biologists
LOX is a lipoxygenase
Acosta I. F., and Farmer E. E. (2008). Jasmonates. In The Arabidopsis Book (The American Society of Plant Biologists), pp. 1-13.
Molecular oxygen is added to
the C13 position by 13-
lipoxygenase (LOX)
© 2015 American Society of Plant Biologists
Allene oxide synthase (AOS)
catalyzes the first committed step
Allene oxide synthase
(AOS) dehydrates 13-
HPOT to form an
unstable allene epoxide
13-HPOT is 13(S)-
hydroxyperoxy-
octadecatrienoic acid
Acosta I. F., and Farmer E. E. (2008). Jasmonates. In The Arabidopsis Book (The American Society of Plant Biologists), pp. 1-13.
© 2015 American Society of Plant Biologists
Allene oxide cyclase (AOC) defines
the stereochemistry
The unstable epoxide
spontaneously forms a
mixture of cis and trans
OPDA BUT, in the presence of
AOC it forms only the
cis form.
Acosta I. F., and Farmer E. E. (2008). Jasmonates. In The Arabidopsis Book (The American Society of Plant Biologists), pp. 1-13.
© 2015 American Society of Plant Biologists
A parallel set of reactions starts with
a 16-carbon fatty acid
Reprinted from Schaller, A., and Stintzi, A. (2009). Enzymes in jasmonate biosynthesis - Structure,
function, regulation. Phytochemistry 70: 1532-1538 with permission from Elsevier.
These reactions take
place in plastids
O
COOH
cis-(+)-OPDA
O
COOH
dnOPDA
© 2015 American Society of Plant Biologists
OPDA and dnOPDA move into the
peroxisome through a transporter
Reprinted from Schaller, A., and Stintzi, A. (2009). Enzymes in jasmonate biosynthesis - Structure,
function, regulation. Phytochemistry 70: 1532-1538 with permission from Elsevier.
The subsequent
reactions take
place in the
peroxisome
CTS / PXA1
O
COOH
cis-(+)-OPDA
O
COOH
dnOPDA
© 2015 American Society of Plant Biologists
In the peroxisome, OPDA is first
reduced and then β-oxidized
Vick, B.A., and Zimmerman, D.C. (1984). Biosynthesis of jasmonic acid by several plant species. Plant Physiol. 75: 458-461.
OPDA reductase (OPR3)
β-oxidation is a multistep
process whose net result is the
removal of two carbon groups
Three cycles of β-
oxidation shorten the 18
carbon OPDA to the 12
carbon jasmonic acid
© 2015 American Society of Plant Biologists
β-oxidation occurs
by the action of
three enzymes
Repeat to
shorten chain
by two more
carbons
OPCL1 OPC-8:CoA ligase 1
Acyl-coenzyme A oxidase (ACX)
Multifunctional protein (MFP)
2-trans-enoyl-CoA hydratase
Multifunctional protein (MFP)
1-3-hydroxyacyl-CoA dehydrogenase
3-ketoacyl-CoA thiolase (KAT)
Li, C., Schilmiller, A.L., Liu, G., Lee, G.I., Jayanty, S., Sageman, C., Vrebalov, J., Giovannoni, J.J., Yagi, K., Kobayashi, Y., and Howe, G.A.
(2005). Role of β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17: 971-986.
© 2015 American Society of Plant Biologists
ACX1 acts during β-oxidation of JA
biosynthesis in the peroxisome
Schilmiller, A.L., Koo, A.J.K. and Howe, G.A. (2007). Functional diversification of acyl-coenzyme A oxidases in
jasmonic acid biosynthesis and action. Plant Physiol. 143: 812-824
ACX1 YFP
YFP
Expression in
pollen of ACX1,
encoding an
enzyme required
for jasmonate
biosynthesis
© 2015 American Society of Plant Biologists
LOX
AOS AOC OPDA OPDA OPR3
β-oxidation
JA
MeJA JA-Ile
plastid peroxisome
Lipase
α-linolenic acid (18:3)
(in membrane)
ACX1
Jasmonic acid is exported to the
cytosol for further modification
© 2015 American Society of Plant Biologists
Jasmonic acid can be conjugated to
amino acids by JAR1
OH
JA JA-Ile
isoleucine
NH2
JAR1
Active
form
JAR1 is an amino
acid conjugase
© 2015 American Society of Plant Biologists
JAR1 was identified as the
jasmonate-insensitive mutant jar1
Staswick, P.E., Su, W., and Howell, S.H. (1992). Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana
mutant. Proc. Natl. Acad. Sci. USA 89: 6837-6840; Staswick, P.E., and Tiryaki, I. (2004). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to
isoleucine in Arabidopsis. Plant Cell 16: 2117-2127.
Arabidopsis jar1 mutants produce jasmonic
acid but cannot make JA-Ile
jar1 mutants are also called far-red insensitive
219 (fin219) due to their phenotype in seedlings
(etiolation under far-red light)
Root growth on
MeJA is less
inhibited in jar1
mutants.
jar1 WT
© 2015 American Society of Plant Biologists
Jasmonate can be reversibly
esterified to MeJA
JA-methyl
transferase
(JMT)
JA MeJA
Methyl
jasmonate
esterase (MJE)
MeJA is volatile and may be
produced for transport
COOH
O
COOCH3
O
© 2015 American Society of Plant Biologists
MeJA production is developmentally
controlled and wound-induced
Seo, H.S., Song, J.T., Cheong, J.-J., Lee, Y.-H., Lee, Y.-W., Hwang, I., Lee, J.S., and Choi, Y.D. (2001). Jasmonic acid carboxyl methyltransferase: A key enzyme
for jasmonate-regulated plant responses. Proc. Natl. Acad. Sci. USA 98: 4788-4793.
JMT expression peaks at
anther dehiscence
JMT is induced by wounding or MeJA
Increased MeJA
production confers
protection against
necrotrophic
pathogens
© 2015 American Society of Plant Biologists
There are other forms of jasmonate
but their functions are not yet known
Swiatek, A., Dongen, W.V., Esmans, E.L., and Onckelen, H.V. (2004). Metabolic Fate of Jasmonates in Tobacco Bright Yellow-2 Cells. Plant Physiol. 135: 161-172.
JA introduced into
cultured cells is
incorporated into
several compounds –
possibly for storage
or degradation?
© 2015 American Society of Plant Biologists
WIPK and SIPK contribute to rapid
activation of JA synthesis enzymes
Kallenbach, M., Alagna, F., Baldwin, I.T., and Bonaventure, G. (2010). Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the
induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiol. 152: 96-106; Bonaventure, G. and Baldwin, I.T. (2010) New
insights into the early biochemical activation of jasmonic acid biosynthesis in leaves. Plant Signal Behaviour 5: 287-289.
WIPK – wound-induced
protein kinase
SIPK – salicylic-acid
induced protein kinase
These protein kinases
might activate enzymes
for very rapid JA
production Stroma
GLA
1
LOX
3
AOS
AOC
glycerolipids
18:3
13(S)-OOH-18:3 OPDA
peroxisome
?
SIPK NPR1 WIPK
OPDA
JA
?
EOT
wounding
chloroplast
© 2015 American Society of Plant Biologists
Cytochrome P450 inactivates JA-Ile
Cytochrome P450 CYP94B3
mediates catabolism
and inactivation of JA-Ile
Koo, A.J., Cooke, T.F., Howe, G.A. (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine. Proc. Natl. Acad. Sci. USA 108: 9298-9303.
Precursor Active Inactive
Loss-of-function
mutant cyp94b3-1
accumulates JA-Ile
© 2015 American Society of Plant Biologists
Control of active hormone levels
LOX
AOS AOC OPDA
OPDA OPR3
β-oxidation
JA
MeJA JA-Ile
Lipase
*
* *
*
Lipases are
developmentally and
wound regulated
AOS and AOC are
wound-regulated (via
a wound-induced
protein kinase)
Entry into peroxisome
may be regulated
JAR1 activity
and JMT activity
are upregulated
by wounding
Jasmonate synthesis is
developmentally regulated as well
Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. (2001). The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing
the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13: 2191-2209.
© 2015 American Society of Plant Biologists
Synthesis, conjugation, transport
and degradation - summary •Jasmonate accumulation is developmentally regulated and
stimulated by wounding, some insects and some pathogens
•Jasmonates are oxylipins, derived from the oxidation of free fatty
acids
•Jasmonate synthesis occurs in plastids and peroxisomes.
Conjugation reactions occur in the cytosol
•JA-Ile is the most active compound whereas MeJA may be a
transport form
•JA-Ile is degraded by cytochrome P450 oxidases
© 2015 American Society of Plant Biologists
Perception and signaling
•JA-Ile binding by the COI1-JAZ coreceptor
•Ubiquitination and degradation of JAZ
•Transcriptional activation by MYC2 and others
Gene expression
SCFCOI1
JA-
Ile
MYC2
BD
AD
JAZ
J
Z
MYC2
BD
AD
© 2015 American Society of Plant Biologists
Coronatine is a bacterial compound
and powerful jasmonate mimic
Reprinted from Weiler, E.W., Kutchan, T.M., Gorba, T., Brodschelm, W., Niesel, U., and Bublitz, F. (1994). The Pseudomonas phytotoxin coronatine mimics octadecanoid
signalling molecules of higher plants. FEBS Letters 345: 9-13 with permission from Elsevier. Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W.,
Luo, H., Nan, F., Wang, Z., and Xie, D. (2009). The Arabidopsis CORONATINE INSENSITIVE1 protein Is a jasmonate receptor. Plant Cell 21: 2220-2236.
MeJA
COR
Control
MeJA or
coronatine
(COR) induce
defense
compounds in
cultured cells of
California poppy
Coronatine is a toxin produced by
some pathogenic bacteria that
mimics jasmonate action and
structurally resembles JA-Ile
(3R,7S)-JA-Ile Coronatine
© 2015 American Society of Plant Biologists
The Arabidopsis mutant coi1 is
insensitive to coronatine and MeJA
Feys, B., Benedetti, C.E., Penfold, C.N., and Turner, J.G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male
sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751-759.
coi1
coi1
WT
WT
MeJA
COR
WT
coi1
Control
© 2015 American Society of Plant Biologists
Tomato jai1 mutant is also deficient
in jasmonate responses
Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E., and Howe, G.A. (2004). The tomato homolog of CORONATINE-INSENSITIVE1
is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
MeJA-resistant
Insect sensitive
Deficient in JA-induced transcription
JAI1 is the tomato
orthologue of COI1
© 2015 American Society of Plant Biologists
Map-based cloning and a functional
assay were used to clone COI1
Functional assay for COI1:
COI1 activity is needed for JA-
or wound-induced activation of
PThi2.1-GUS reporter
construct.
(Thionins are JA-induced
defense proteins)
From Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G. (1998). COI1: An Arabidopsis gene required for
jasmonate-regulated defense and fertility. Science 280: 1091-1094. Reprinted with permission from AAAS.
© 2015 American Society of Plant Biologists
Genetic mapping led to two candidate genes and the
functional assay showed which has COI1 activity
From Xie, D.-X., Feys, B.F., James, S., Nieto-Rostro, M., and Turner, J.G. (1998). COI1: An Arabidopsis gene required for
jasmonate-regulated defense and fertility. Science 280: 1091-1094. Reprinted with permission from AAAS.
YES YES YES NO
Genetic complementation of
coi1 mutant by COI1 gene
© 2015 American Society of Plant Biologists
Reprinted from Katsir, L., Chung, H.S., Koo, A.J.K., and Howe, G.A. (2008). Jasmonate signaling: a conserved
mechanism of hormone sensing. Curr. Opin. Plant Biol. 11: 428-435, with permission from Elsevier.
This similarity suggests a mode
of action!
COI1 is closely related to TIR1 and
other auxin receptors (AFB)
F-box proteins COI1 protein
family (jasmonate
coreceptors)
TIR1 / AFB
protein family
(auxin receptors)
Reprinted from Chico, J.M., Chini, A., Fonseca, S., and Solano, R. (2008). JAZ repressors set the rhythm
in jasmonate signaling. Curr. Opin. Plant Biol. 11: 486-494 with permission from Elsevier.
© 2015 American Society of Plant Biologists
The jasmonate receptor consists of
COI1 and JAZ co-receptors
Reprinted by permission from Macmillan Publishers Ltd. Nature: Sheard, L.B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds,
T.R., Kobayashi, Y., Hsu, F.-F., Sharon, M., Browse, J., He, S.Y., Rizo, J., Howe, G.A., and Zheng, N. (2010) Jasmonate perception by
inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400-405 copyright 2010.
COI1 JA-
Ile
The COI1-JAZ co-receptor has > 100
fold greater affinity for the ligand than
either COI1 or JAZ alone
© 2015 American Society of Plant Biologists
COI1 is a component of the SCF
ubiquitin ligase complex SCFCOI1
CUL1
SKP1
F-box COI1
protein
COI1 F-box
protein
SCF complex
SCF ubiquitin ligase complex
(Named for SKP1, CUL1 and F-box
proteins)
(The auxin receptor TIR1 is a component of the SCFTIR1 complex)
© 2015 American Society of Plant Biologists
Ubiquitin ligase complexes
ubiquitinate target proteins
The F-box protein recognizes
and binds to the target protein.
The complex then transfers
ubiquitin proteins to the target
CUL1
SKP1
Target Target
Ubiquitin
F-box
protein
© 2015 American Society of Plant Biologists
Proteolytic targets are covalently
linked to ubiquitin
Ubiquitin by Rogerdodd
Ubiquitin Ubiquitin is a small (76 aa)
protein that targets proteins
for proteolytic degradation Target
© 2015 American Society of Plant Biologists
Ubiquitinated targets are
proteolyzed by the 26S proteasome
26S proteasome
The proteasome
breaks down target
proteins and recycles
ubiquitin
Target
© 2015 American Society of Plant Biologists
Jasmonate (like auxin) signaling
requires repressor degradation
Repressor
Transcriptional
activator
JAZ
MYC2
Aux/IAA
ARF
F-box
protein TIR1 COI1
hormone
Repressor
Transcriptional
activator
Auxin JA-Ile
JAZ
MYC2
Aux/IAA
ARF
+ hormone
In the absence of hormone, a
repressor interferes with a
transcriptional activator. The hormone
promotes an interaction between the
repressor and an F-box protein,
leading to repressor degradation and
transcriptional activation
© 2015 American Society of Plant Biologists
JAZ proteins are repressors of
jasmonate signaling
Reprinted from Chung, H.S., Niu, Y., Browse, J., and Howe, G.A. (2009). Top hits in contemporary JAZ: An update on jasmonate
signaling. Phytochemistry 70: 1547-1559 with permission from Elsevier.
© 2015 American Society of Plant Biologists
JAZ proteins are rapidly degraded in
the presence of jasmonates
Reprinted by permission from Macmillan Publishers Ltd. [Nature] Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A.,
and Browse, J. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665. and Chini, A., Fonseca, S.,
Fernandez, G., Adie, B., Chico, J.M., Lorenzo, O., Garcia-Casado, G., Lopez-Vidriero, I., Lozano, F.M., Ponce, M.R., Micol, J.L., and Solano, R. (2007). The JAZ family
of repressors is the missing link in jasmonate signalling. Nature 448: 666-671 copyright 2007.
Control
+ jasmonate
Protein stability was
assayed in transgenic
plants expressing
JAZ-GFP or JAZ-GUS
fusions
JAZ-GFP
© 2015 American Society of Plant Biologists
JAZ genes are transcriptionally
upregulated by jasmonates
Reprinted by permission from Macmillan Publishers Ltd. [Nature] Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A.,
and Browse, J. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665.
Many JAZ genes are rapidly
induced by JA application
Similarly, transcription of the
Aux/IAA repressor genes are
rapidly upregulated by auxin
© 2015 American Society of Plant Biologists
JAZ proteins have conserved Jas
and ZIM/TIFY domains
Chung, H.S., and Howe, G.A. (2009). A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-
domain protein JAZ10 in Arabidopsis. Plant Cell 21: 131-145.
The Jas domains facilitate
interactions with COI1 and
MYC2 proteins. The ZIM
domains (also called TIFY
domains) are dimerization
domains for interactions
with other JAZ proteins and
NINJA
© 2015 American Society of Plant Biologists
In the jai3-1 mutant, the JAI3 protein
lacks a Jas domain
Reprinted by permission from Macmillan Publishers Ltd. [Nature] Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J.M., Lorenzo, O., Garcia-Casado, G.,
Lopez-Vidriero, I., Lozano, F.M., Ponce, M.R., Micol, J.L., and Solano, R. (2007). The JAZ family of repressors is the missing link in jasmonate signalling.
Nature 448: 666-671 copyright 2007.
A mutation changes the
encoded protein so it
lacks the Jas domain
and no longer interacts
with COI1.
Therefore it is not
degraded and continues
to repress JA responses
including root inhibition
by MeJA
jasmonate-
insensitive3
SCFCOI1
JA-
Ile
© 2015 American Society of Plant Biologists
Plants expressing stabilized JAZ are
deficient in insect defenses
Chung, H.S., Koo, A.J.K., Gao, X., Jayanty, S., Thines, B., Jones, A.D., and Howe, G.A. (2008). Regulation and function of Arabidopsis
JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 146: 952-964.
Plants with stabilized
JAZ proteins are
deficient in defense
responses. This is
clearly seen by the
growth rate of insects
feeding on them!
© 2015 American Society of Plant Biologists
The JAZ ZIM domain facilitates
interactions with NINJA
Image by Hector Gomez
JAZ
Jas
ZIM NINJA
NINJA = Novel Interactor of JAZ
And NINJA interacts with TOPLESS......
© 2015 American Society of Plant Biologists
TOPLESS represses transcription in
absence of hormones
TPL
ARF
BD
III/IV
Aux/IAA
III/IV
EAR
TOPLESS binds directly to the
EAR domain of the Aux/IAA
repressors
TPL
JAZ
J
Z
NINJA
MYC2
BD
AD
EAR
TOPLESS binds indirectly to JAZ,
through NINJA
© 2015 American Society of Plant Biologists
Direct targets of JAZ and downstream
regulation of transcription factors
Reprinted from Kazan, K., Manners, J.M. (2011). JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 17: 22-31, with permission from Elsevier.
© 2015 American Society of Plant Biologists
The auxin signaling pathway
SCFTIR1
IAA
IAA
TPL
ARF
BD
III/IV
Aux/IAA III/IV
EAR
Aux/IAA III/IV
EAR
1. Auxin binds to SCFTIR1
and Aux/IAA
© 2015 American Society of Plant Biologists
The auxin signaling pathway
SCFTIR1
IAA
IAA
TPL
ARF
BD
III/IV
Aux/IAA III/IV
EAR
1. Auxin binds to SCFTIR1
and Aux/IAA
2. Aux/IAA
ubiquitinated and
degraded by 26S
proteasome
© 2015 American Society of Plant Biologists
The auxin signaling pathway
BD
AD
SCFTIR1
IAA
IAA
TPL
ARF
BD
III/IV
Aux/IAA III/IV
EAR
1. Auxin binds to SCFTIR1
and Aux/IAA
2. Aux/IAA
ubiquitinated and
degraded by 26S
proteasome
3. Degradation of
repressor permits
transcriptional
activation by ARF
transcription
factors ARF
© 2015 American Society of Plant Biologists
The jasmonate signaling pathway
JA-Ile
TPL JAZ
J
Z
NINJA
MYC2
BD
AD
EAR
1.JA-Ile binds to SCFCOI1
and JAZ protein
SCFCOI1
JA-
Ile
© 2015 American Society of Plant Biologists
The jasmonate signaling pathway
SCFCOI1
JA-Ile
TPL JAZ
J
Z
NINJA
MYC2
BD
AD
EAR
1.JA-Ile binds to SCFCOI1
and JAZ protein
2. JAZ
ubiquitinated and
degraded by 26S
proteasome
JA-
Ile
© 2015 American Society of Plant Biologists
The jasmonate signaling pathway
BD
AD
SCFCOI1
JA-Ile
TPL JAZ
J
Z
NINJA
MYC2
BD
AD
EAR
1.JA-Ile binds to SCFCOI1
and JAZ protein
2. JAZ
ubiquitinated and
degraded by 26S
proteasome
3. Degradation of
repressor permits
transcriptional
activation by MYC2
transcription factors MYC2
JA-
Ile
© 2015 American Society of Plant Biologists
jin1 is deficient in JA-induced
transcription and encodes MYC2
Berger, S., Bell, E., and Mullet, J.E. (1996). Two methyl jasmonate-insensitive mutants show altered expression of AtVsp in response to methyl jasmonate and
wounding. Plant Physiol. 111: 525-531; Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC
transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
AtVSP mRNA
MYC2 upregulates:
JAZ genes
LOX3 (JA synthesis)
VSP2 (wound response)
MYC2 MYC2
© 2015 American Society of Plant Biologists
MYC2 downregulates some
pathogen-response genes
Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate
between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
MYC2
© 2015 American Society of Plant Biologists
JA-regulated genes can be
positively or negatively regulated by
ethylene
Reprinted from Memelink, J. (2009). Regulation of gene expression by jasmonate hormones. Phytochemistry 70: 1560-1570 with permission from Elsevier.See also Zhu, Z., et al., (2011).
Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 12539–12544.
PDF1.2 requires both
JA and ethylene
VSP1 is down
regulated by ethylene
© 2015 American Society of Plant Biologists
The Mediator complex is a key
regulator of JA-dependent defense
Kidd, B.N., Edgar, C.I., Kumar, K.K., Aitken, E.A., Schenk, P.M., Manners, J.M. and Kazan, K. (2009). The Mediator Complex
subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell. 21: 2237-2252.
The Mediator
complex acts as a
bridge between RNA
polymerase II and
transcription factors
and fine-tunes
diverse regulatory
inputs
© 2015 American Society of Plant Biologists
Core jasmonate signaling –
summary
BD
AD
SCFCOI1
JA-Ile
TPL JAZ
J
Z
NINJA
MYC2
BD
AD
EAR
1.JA-Ile binds to SCFCOI1
and JAZ protein
2. JAZ
ubiquitinated and
degraded by 26S
proteasome
3. Degradation of
repressor permits
transcriptional
activation by MYC2
and other
transcription factors MYC2
JA-
Ile
There is also
extensive cross-talk
with other signaling
pathways!
© 2015 American Society of Plant Biologists
Jasmonates in whole-plant
processes
•Responses to insects
•Responses to pathogens
and other microorganisms
•Cross-talk between JA and
SA pathways
•Jasmonates in development
and other processes
Mithofer, A., and Boland, W. (2008). Recognition of herbivory-associated molecular patterns. Plant Physiol. 146: 825-831.
© 2015 American Society of Plant Biologists
Plants and insects have shared a
long period of co-evolution
> 400 mya
Image credit: L. Shyamal based on work by Bruce Tiffney
© 2015 American Society of Plant Biologists
Plants are not passive victims
Direct responses – production of toxic or
anti-nutritive compounds (e.g. proteinase
inhibitors)
Indirect responses – volatile compounds
recognized by carnivorous or parasitoid
insects
Plants have constitutive and induced defenses
Induced responses can be direct or indirect
Constitutive – always present
Chemical – toxins, irritants (e.g.
cyanogenic glycosides, alkaloids,
tannins)
Physical – thorns, trichomes Linamarin, a cyanogenic
glycoside from cassava
Geocoris feeding on
Manduca eggs, attracted
by plant-emitted volatiles
Trichome photo credit: NRC-CNRC (Harry Turner) . Geocoris photo by M. Stitz from Allmann, S., and Baldwin, I.T. Insects betray themselves in nature to
predators by rapid Isomerization of green leaf volatiles. Science 329: 1075-1078 reprinted with permission from AAAS.
© 2015 American Society of Plant Biologists
There are many kinds of arthropods
and feeding behaviors
Image credits: Syncroscopy; David Riley; N3v3rl4nd; Mithofer, A., and Boland, W. (2008). Recognition of herbivory-associated molecular patterns. Plant Physiol. 146: 825-831.
S. littoralis caterpillar feeding on
a barrel medic (Medicago
truncatula) leaf
Adult green peach aphid
(Myzus persicae) feeding on
a dill plant
Tomato leaf showing
damage caused by a
leaf miner
Beet armyworm (Spodoptera
exigua) damage to sweet
pepper (Capsicum annuum)
© 2015 American Society of Plant Biologists
Plants respond to oral secretions as
well as mechanical damage
Korth, K.L., and Dixon, R.A. (1997). Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiol. 115: 1299-1305.
Proteinase inhibitor gene
induction is much faster
when insect saliva or
regurgitate is present Plants recognize insect-
derived compounds as well as
mechanical damage
© 2015 American Society of Plant Biologists
Plants produce proteinase
inhibitors that deter and weaken
herbivores
Green, T.R., and Ryan, C.A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175: 776-777.
Photo courtesy of Washington State University and Scott Bauer, USDA
In 1972, Green & Ryan found that
plants produce proteinase inhibitors
(PIs) in response to herbivory
47 202 A four-fold increase
in PIs was recorded
after 24 hours
Control plant Plant infested with herbivore
Clarence Ryan (1931-2007) was a
pioneer in the study of plant
responses to herbivorous insects
© 2015 American Society of Plant Biologists
Plants produce proteinase inhibitors
that interfere with digestion
Normally food that
enters the digestive
system is broken down
by digestive enzymes
so the nutrients can be
absorbed
MUNCH
MUNCH
Green, T.R., and Ryan, C.A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175: 776-777.
© 2015 American Society of Plant Biologists
Plants produce proteinase inhibitors
that interfere with digestion
Proteinase
inhibitors (PIs)
make insects sick
or even die
I feel sick
Green, T.R., and Ryan, C.A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175: 776-777.
© 2015 American Society of Plant Biologists
Jamonate signaling contributes to
defenses against herbivory WT Mutant without JA
When exposed to hungry
fly larvae, plants unable
to produce JA have low
rates of survival
McConn, M., Creelman, R.A., Bell, E., Mullet, J.E., and Browse, J. (1997). Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94: 5473-5477.
© 2015 American Society of Plant Biologists
Jasmonates accumulate extremely
quickly after wounding
Glauser, G., Dubugnon, L., Mousavi, S.A.R., Rudaz, S., Wolfender, J.-L., and Farmer, E.E. (2009). Velocity estimates for signal
propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 284: 34506-34513.
Unwounded
plant
W (wounded)
part of leaf
U (unwounded)
part of leaf
When a leaf is crushed
with forceps, the level
of JA in the wounded
and unwounded part of
the leaf increases
within a minute
© 2015 American Society of Plant Biologists
The defense responses occurs in
unwounded leaves as well
336 103
Elevated PIs were
recorded from
unwounded leaves
as well suggesting
a mobile signal
Control plant Plant infested with herbivore –
extract from distant leaf
Green, T.R., and Ryan, C.A. (1972). Wound-induced proteinase inhibitor in plant leaves: A possible defense mechanism against insects. Science 175: 776-777.
© 2015 American Society of Plant Biologists
PI genes are induced by jasmonate
treatment, locally and systemically
Farmer, E.E., Johnson, R.R., and Ryan, C.A. (1992). Regulation of expression of proteinase inhibitor
genes by methyl jasmonate and jasmonic acid. Plant Physiol. 98: 995-1002.
244 103
6 2
Proteinase inhibitor gene
expression is induced by
Wounding or Methyl
Jasmonate.
MeJA vapor promotes PI
accumulation in exposed
leaves but also
unexposed leaves of the
same plant No MJ control
© 2015 American Society of Plant Biologists
Systemic signaling does not involve
movement of JA-Ile but may involve
other jasmonates
Wang, L., Allmann, S., Wu, J., and Baldwin, I.T. (2008). Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic
acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol. 146: 904-915.
The nature of the mobile signal is
still not resolved – it may include:
•Jasmonates
•Hydraulic signals
•Ionic signals
© 2015 American Society of Plant Biologists
Tomatoes and related plants
produce systemin, a peptide signal
Ryan, C.A., and Pearce, G. (2003). Systemins: A functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc. Natl. Acad.
Sci. USA 100: 14577-14580 copyright 2003 National Academy of Sciences USA.
Systemin is produced by
cleavage of a larger
protein prosystemin
© 2015 American Society of Plant Biologists
Expression of systemin in the
rootstock induces PIs in the scion
McGurl, B., Orozco-Cardenas, M., Pearce, G., and Ryan, C.A. (1994). Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic
signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 91: 9799-9802.
WT
35S:
Prosys
Initially these data
suggested that
systemin itself is the
mobile signal, but we
now believe
systemin’s role is only
at the wound site
220
273
WT
WT
13
15
© 2015 American Society of Plant Biologists
The COI1 receptor is required at the
systemic site but JA synthesis is not
WT
WT
13
15
35S:
Prosys
279
jai1
(COI1
receptor
mutant)
0
35S:
Prosys
spr-2
(JA
synthesis
mutant)
263
150
McGurl, B., Orozco-Cardenas, M., Pearce, G., and Ryan, C.A. (1994). Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic
signal that constitutively induces proteinase inhibitor synthesis. Proc. Natl. Acad. Sci. USA 91: 9799-9802.
© 2015 American Society of Plant Biologists
Systemin at the wound site generates or
amplifies the systemic signal
Li, L., Li, C., Lee, G.I., and Howe, G.A. (2002). Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc. Natl.
Acad. Sci. USA 99: 6416-6421 copyright 2002 National Academy of Sciences USA.
The mobile signal (“X”) is
still being debated
© 2015 American Society of Plant Biologists
Indirect responses include volatile
compounds that attract carnivorous
and parasitic insects
Tim Haye, Universität Kiel, Germany Bugwood.org; R.J. Reynolds Tobacco Company Slide Set and R.J. Reynolds Tobacco Company, Bugworld.org
And insects that
lay their eggs in
the herbivore,
which gets eaten
when they
hatch!
Volatiles attract
carnivorous
insects that eat
the herbivore
© 2015 American Society of Plant Biologists
Charles Darwin had thoughts about
parasitic insects
I cannot persuade myself that a beneficent
and omnipotent God would have designedly
created the Ichneumonidae with the express
intention of their feeding within the living
bodies of caterpillars.
– Charles Darwin, 1860
© 2015 American Society of Plant Biologists
Jasmonate mediates defenses
against necrotrophic pathogens
Photo credit Gary Loake
Arabidopsis plants infected with Botrytis cinerea
© 2015 American Society of Plant Biologists
JA-insensitive plants are more
susceptible to pathogens
Thomma, B.P.H.J., Eggermont, K., Penninckx, I.A.M.A., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A., and Broekaert, W.F. (1998). Separate jasmonate-dependent
and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA 95: 15107-
15111 copyright 1998 National Academy of Sciences USA.
Alternaria
brassicicola
Botrytis
cinerea
© 2015 American Society of Plant Biologists
JA-induces plant defenses against
pathogens
Photo credit: USDA
Peanut kernel infected by a soil fungus (Aspergillus
niger). Yellow-colored phytoalexin is locally produced by
the kernel tissues (arrow)
JA-mediated responses to
pathogens include production of
phytoalexins, and antimicrobial
peptides or proteins
© 2015 American Society of Plant Biologists
Jasmonates protect plants through
induced resistance
Adapted from Frost, C.J., Mescher, M.C., Carlson, J.E., and De Moraes, C.M. (2008). Plant defense priming against herbivores: Getting ready for a different battle. Plant Physiol. 146: 818-824;
Conrath, U., Beckers, G.J.M., Flors, V., García-Agustín, P., Jakab, G.b., Mauch, F., Newman, M.-A., Pieterse, C.M.J., Poinssot, B., Pozo, M.J., Pugin, A., Schaffrath, U., Ton, J., Wendehenne, D.,
Zimmerli, L., and Mauch-Mani, B. (2006). Priming: Getting ready for battle. Mol. Plant-Microbe Interact. 19: 1062-1071.
Beneficial
bacteria or
fungi
Prior exposure to a pest, or
colonization with some non-
pathogenic bacteria can prime a
plant for enhanced responses.
Pseudomonas fluorescens
WCS417r primes the plant
to elicit a stronger, faster
response to MeJA
© 2015 American Society of Plant Biologists
The mechanisms of priming are not
fully understood
Reprinted from Conrath U. (2011). Molecular aspects of defence priming. Trend Plant Sci 16: 524-531 with permission from Elsevier.
Perhaps signaling
molecules or transcription
factors increase in an
abundant, inactive state,
leading to an enhanced
defense response upon
subsequent attack
© 2015 American Society of Plant Biologists
JA seems to play a role in
establishing mutualistic interactions
Reprinted from Hause, B., and Schaarschmidt, S. (2009). The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry
70: 1589-1599 with permission from Elsevier.
Arbuscular mycorrhiza Legume-rhizobia
symbiosis
© 2015 American Society of Plant Biologists
Cross-talk between JA and SA-
mediated signaling
Jasmonates Salicylates
Remarkably, there is
considerable cross-
talk between JA and
SA signaling
pathways
© 2015 American Society of Plant Biologists
Exogenous application of SA
enhances success of an herbivore
Cui, J., Bahrami, A.K., Pringle, E.G., Hernandez-Guzman, G., Bender, C.L., Pierce, N.E., and Ausubel, F.M. (2005). Pseudomonas syringae manipulates systemic plant
defenses against pathogens and herbivores. Proc. Natl. Acad. Sci. USA 102: 1791-1796 copyright 2005 National Academy of Sciences USA.
Trichoplusia ni (cabbage
looper) herbivory is enhanced
by SA and inhibited by MeJA
© 2015 American Society of Plant Biologists
Salicylates repress jasmonate
signaling
Koornneef, A., and Pieterse, C.M.J. (2008). Cross talk in defense signaling. Plant Physiol. 146: 839-844.
JA-induced
SA-induced
JA
PDF1.2 PR-1
SA
JA induces expression of PDF1.2, but
in the presence of JA + SA the gene is
not activated. SA overrides JA.
© 2015 American Society of Plant Biologists
Some insects induce SA responses
and repress JA responses
Zarate, S.I., Kempema, L.A., and Walling, L.L. (2007). Silverleaf whitefly induces salicylic acid
defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143: 866-875.
Silverleaf whitefly nymphs
induce SA defenses which
suppress JA defenses,
increasing their survival - +
SA-induced
JA-induced
JA-induced
© 2015 American Society of Plant Biologists
Salicylates also make plants more
susceptible to necrotrophs
Spoel, S.H., Johnson, J.S., and Dong, X. (2007). Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of
the National Academy of Sciences 104: 18842-18847 copyright National Academy of Sciences USA.
SA tends to
override JA-
mediated
responses
The necrotrophic fungus
Alternaria brassicicola
reproduces better on
Arabidopsis plants treated
with salicylic acid (SA)
JA
PDF1.2 PR-1
SA
© 2015 American Society of Plant Biologists
NONEXPRESSER OF
PR GENES1 (NPR1) is
activated by SA, and
interferes with JA
signaling
The Mediator complex
subunit16 (MED16) has
been implicated with this
signaling pathway
(downstream of NPR1) in
order to call RNA Pol II
and initiate transcription
NPR1 is a node through which SA
and JA pathways intersect
Spoel, S.H. et al. (2003). NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770. Zhang, X. et al. (2012). The
Arabidopsis Mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24: 4294-4309.
RNA Pol II
MED16
© 2015 American Society of Plant Biologists
Coronatine stimulates JA responses,
suppressing SA response
JA SA
Coronatine-
producing
bacterium
Defense Coronatine is an excellent
mimic of JA-Ile. Production of
coronatine significantly
enhances the pathogenicity of
bacteria that produce it
© 2015 American Society of Plant Biologists
Different pathogens elicit different
“signal signatures”
De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Metraux, J.-P., Van Loon, L.C., Dicke, M., and Pieterse,
C.M.J. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18: 923-937.
Plants are able to perceive the type of pathogen
or pest threatening them, and respond in
different, appropriate ways.
We still don’t understand much of this recognition
process
© 2015 American Society of Plant Biologists
Ethylene and jasmonate pathways
confer specificity to the response
Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate
between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950.
Pathogens induce ethylene and
jasmonate production, and activate a
different subset of genes as those
induced by wounding or herbivory
© 2015 American Society of Plant Biologists
Defense pathways coordinate with
ABA and developmental signals
Reprinted from Spoel, S.H., and Dong, X. (2008) Making sense of hormone crosstalk during plant
immune responses. Cell Host Microbe 3: 348-351 with permission from Elsevier.
© 2015 American Society of Plant Biologists
Jasmonates integrate signals in
plant growth and development
Wasternack, C., and Hause, B. (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and
development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111: 1021–1058 by permission of Oxford University Press.
Root growth inhibition Tuber formation Senescence
Trichome formation Flower development
© 2015 American Society of Plant Biologists
Jasmonates contribute to
developmental and growth controls
Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Pichersky, E., and Howe, G.A. (2004). The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed
maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143; Reprinted by permission from Macmillan Publishers Ltd. Thines, B., Katsir, L., Melotto, M., Niu, Y.,
Mandaokar, A., Liu, G., Nomura, K., He, S.Y., Howe, G.A., and Browse, J. (2007). JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665.
Flower development
JA also controls: cell cycle, root
extension, leaf senescence,
stomata closure, and mutualistic
interactions....
Trichome formation Seed development
© 2015 American Society of Plant Biologists
Qi, T., Huang, H., Song, S., and Xie, D. (2015). Regulation of jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell. 27: 1620-1633
GA antagonizes positive effect of JA on
stamen development
JA regulates stamen development
© 2015 American Society of Plant Biologists
Jasmonates and nutrients
Jasmonates promote
nutrient reallocation
away from leaves into
roots
Jasmonates promote
tuber formation in potato
Potassium-starved
Arabidopsis accumulate
jasmonates and are more
resistant to insects
There is a connection between jasmonates,
nutrients and energy reserves that may
contribute to defense and survival
Armengaud, P., Breitling, R., and Amtmann, A. (2010) Coronatine-Insensitive 1 (COI1) mediates transcriptional responses of Arabidopsis thaliana to
external potassium supply. Mol. Plant 3: 390-405.
© 2015 American Society of Plant Biologists
Control of primary root development
involves both auxin and jasmonate
Reprinted from Kazan, K., Manners, J.M. (2011). JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 17: 22-31, with permission from Elsevier;
Reprinted with permission from Hoffmann, M., Hentrich, M., Pollmann, S. (2011). Auxin-oxylipin crosstalk: Relationship of antagonists. J. Integr. Plant Biol. 53: 429–445.
© 2015 American Society of Plant Biologists
Auxin and jasmonate act
antagonistically on leaf senescence
Reprinted from Jian et al. (2014). Arabidopsis WRKY functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic-acid induced leaf senescence. Plant Cell 26: 230-245
Ultimately, via WRKY57
JA induces leaf senescence
Auxin suppresses leaf senescence
© 2015 American Society of Plant Biologists
Ethylene and JA act antagonistically on
apical hook formation
Zhang, X et al. (2014). Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell. 26: 1105-1117.
EIN3 is induced by ethylene, and will
ultimately induce apical hook formation.
On the other hand, JA-induced MYC2
and EBF1 repress EIN3 activity,
inhibiting apical hook formation by
repressing expression of HLS1
© 2015 American Society of Plant Biologists
Competition between GA and JA
Reprinted from Kazan, K., Manners, J.M. (2011). JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 17: 22-31, with permission from Elsevier.
See also Hou, X. et al. (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZ. Dev. Cell 19: 884-894
Normal
situation –
growth and
defense are
balanced
DELLAs competing
with MYCs for JAZs
binding while JAZs
competing with PIFs
for DELLA binding
Elevated JA -
defense
Elevated GA -
growth
© 2015 American Society of Plant Biologists
Jasmonates integrate with light
signals via JAZ and and JAR1
Hsieh, H.L., and Okamoto, H. (2014). Molecular interaction of jasmonate and phytochrome A signalling. J Exp Bot. 65: 2847-2857 by permission of Oxford University Press; Robson, F., Okamoto, H., Patrick, E.,
Harris, S.-R., Wasternack, C., Brearley, C. and Turner, J.G. (2010). Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell. 22: 1143-1160.
© 2015 American Society of Plant Biologists
Ongoing questions
JA
MeJA JA-Ile
What signals trigger JA synthesis and
signaling pathways?
How does the plant discriminate
between threats?
What is the systemic signal?
What do the different JAZ proteins do?
How is the diversity of JA responses
controlled in specific organs and cell
types?
COI1 JA-
Ile
© 2015 American Society of Plant Biologists
How does the plant prioritize its
stress and defense responses?
Pathogens (biotrophs)
Biotic stress
SA ABA
Stress-response
genes
SA-response
genes
Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., and Solano, R. (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to
discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938-1950. Robert-Seilaniantz, A., Grant, M., Jones, J.D.G.
(2011). Hormone crosstalk in plant disease and defense: More than just JASMONATE-SALICYLATE antagonism. Annu. Rev. Phytopathol. 49: 317–343.
© 2015 American Society of Plant Biologists
How can plant scientists prevent
crop losses to disease and insects?
Photo credit: ARS USDA
Most plants are resistant to most pests.
Nevertheless, pre- and post-harvest
crops losses can be devastating.
Understanding jasmonates helps plant
scientists and breeders enhance plant
resistance and optimize development